Legged locomotion of animals and humans is controlled by a complex network of neurons. Proposed in the early 20th century [Brown, T. G., 1914. On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. J Physiol 48 (1), 18-46.]. and firmly established today [Orlovsky, G., Deliagina, T., Grillner, S., 1999. Neuronal control of locomotion: from mollusc to man. Oxford University Press, New York], the central pattern generator (CPG) forms the basis of this network.
In the current view, the CPG consists of layers of neuron pools in the spinal cord [Rybak, I. A., Shevtsova, N. A., Lafreniere-Roula, M., McCrea, D. A., 2006. Modelling spinal circuitry involved in locomotor pattern generation: insights from deletions during fictive locomotion. J Physiol 577 (Pt 2), 617-639] which, through other neuron pools channeling muscle synergies, provide rhythmic activity to the leg extensor and flexor muscles [Dietz, V, 2003. Spinal cord pattern generators for locomotion. Clin Neurophysiol 114 (8), 1379-1389; Minassian, K., Persy, I., Rattay, F., Pinter, M. M., Kern, H., Dimitrijevic, M. R., 2007. Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity. Hum Mov Sci 26 (2), 275-295] sufficient to generate stepping movements, even in the absence of spinal reflexes [Grillner, S., Zangger, P., 1979. On the central generation of locomotion in the low spinal cat. Exp Brain Res 34 (2), 241-261; Frigon, A., Rossignol, S., 2006. Experiments and models of sensorimotor interactions during locomotion. Biol Cybern 95 (6), 607-627]. Spinal reflexes are nevertheless part of this complex network [Rybak, I. A., Stecina, K., Shevtsova, N. A., McCrea, D. A., 2006. Modelling spinal circuitry involved in locomotor pattern generation: insights from the effects of afferent stimulation. J Physiol 577 (Pt 2), 641-658], contributing to the selection of locomotive patterns, the timing of the extensor and flexor activities, and the modulation of the CPG output.
Using this combination of a central pattern generation and modulating reflexes, neuromuscular models of lampreys [Ekeberg, O., Grillner, S., 1999. Simulations of neuromuscular control in lamprey swimming. Philos Trans R Soc Lond B Biol Sci 354 (1385), 895-902], salamanders [Ijspeert, A., Crespi, A., Ryczko, D., Cabelguen, J.-M., 2007. From swimming to walking with a salamander robot driven by a spinal cord model. Science 315 (5817), 1416-1420], cats [Ivashko, D. G., Prilutski, B. I., Markin, S. N., Chapin, J. K., Rybak, I. A., 2003. Modeling the spinal cord neural circuitry controlling cat hindlimb movement during locomotion. Neurocomputing 52-54, 621-629; Yakovenko, S., Gritsenko, V, Prochazka, A., 2004. Contribution of stretch reflexes to locomotor control: a modeling study. Biol Cybern 90 (2), 146-155; Maufroy, C., Kimura, H., Takase, K., 2008. Towards a general neural controller for quadrupedal locomotion. Neural Netw 21(4), 667-681], and humans [Ogihara, N., Yamazaki, N., 2001. Generation of human bipedal locomotion by a bio-mimetic neuro-musculo-skeletal model. Biol Cybern 84 (1), 1-11; Paul, C., Bellotti, M., Jezernik, S., Curt, A., 2005. Development of a human neuro-musculo-skeletal model for investigation of spinal cord injury. Biol Cybern 93 (3), 153-170] have developed into essential tools for studying different control strategies in animal and human locomotion. The emphasis of these models has been to reproduce the architecture of the CPG and underlying reflexes suggested by experiments [Pearson, K., Ekeberg, O., Buschges, A., 2006. Assessing sensory function in locomotor systems using neuro-mechanical simulations. Trends Neurosci 29 (11), 625-631]. However, little attention has been paid to understanding how such architectures might represent or encode principles of locomotion mechanics.
These principles suggest that, in contrast to the complexity of the identified neural networks, legged locomotion requires little or no control. For instance, two conceptual models of walking [Alexander, R., 1976. Mechanics of bipedal locomotion. In: Perspectives in experimental biology (Ed. Davies, P. S.) Pergamon, Oxford; Mochon, S., McMahon, T., 1980. Ballistic walking. J. Biomech. 13 (1), 49-57] and running [Blickhan, R., 1989. The spring-mass model for running and hopping. J. of Biomech. 22, 1217-1227; McMahon, T., Cheng, G., 1990. The mechanism of running: how does stiffness couple with speed? J. of Biomech. 23, 65-78] have been put forth that capture dominant mechanisms of legged locomotion. Researchers have demonstrated the capacity of these models to self-stabilize if the mechanical system is properly tuned [McGeer, T., 1990. Passive dynamic walking. Int. J. Rob. Res. 9 (2), 62-82; McGeer, T., 1992. Principles of walking and running. Vol. 11 of Advances in Comparative and Environmental Physiology. Springer-Verlag Berlin Heidelberg, Ch. 4; Seyfarth, A., Geyer, H., Günther, M., Blickhan, R., 2002. A movement criterion for running. J. of Biomech. 35, 649-655; Ghigliazza, R., Altendorfer, R., Holmes, P., Koditschek, D., 2003. A simply stabilized running model. SIAM J. Applied. Dynamical Systems 2 (2), 187-218]. Walking and running robots have moreover demonstrated the practical relevance and control benefits derived from this principle [Raibert, M., 1986. Legged robots that balance. MIT press, Cambridge; McGeer, T., 1990. Passive dynamic walking. Int. J. Rob. Res. 9 (2), 62-82; Saranli, U., Buehler, M., Koditschek, D., 2001. Rhex: A simple and highly mobile hexapod robot. Int. Jour. Rob. Res. 20(7), 616-631; Collins, S., Ruina, A., Tedrake, R., Wisse, M., 2005. Efficient bipedal robots based on passive-dynamic walkers. Science 307 (5712), 1082-1085]. But it remains an open question how this and other principles of legged mechanics are integrated into the human motor control system.
The importance of this interplay between mechanics and motor control has been recognized by neuroscientists and biomechanists alike [Pearson, K., Ekeberg, O., Buschges, A., 2006. Assessing sensory function in locomotor systems using neuro-mechanical simulations. Trends Neurosci 29 (11), 625-631]. For instance, although it is generally accepted that the CPG forms a central drive for motor activity in locomotion [Grillner, S., Zangger, P., 1979. On the central generation of locomotion in the low spinal cat. Exp Brain Res 34 (2), 241-261; Dietz, V, 2003. Spinal cord pattern generators for locomotion. Clin Neurophysiol 114 (8), 1379-1389; Frigon, A., Rossignol, S., 2006. Experiments and models of sensorimotor interactions during locomotion. Biol Cybern 95 (6), 607-627; Ijspeert, A. J., 2008. Central pattern generators for locomotion control in animals and robots: a review. Neural Netw 21(4), 642-653], Lundberg suggested in 1969 that, out of its rather simple central input, spinal reflexes, which relay information about locomotion mechanics, could shape the complex muscle activities seen in real locomotion [Lundberg, A., 1969. Reflex control of stepping. In: The Nansen memorial lecture V, Oslo: Universitetsforlaget, 5-42]. Refining this idea, Taga later proposed that, because “centrally generated rhythms are entrained by sensory signals which are induced by rhythmic movements of the motor apparatus . . . [,] motor output is an emergent property of the dynamic interaction between the neural system, the musculo-skeletal system, and the environment” [Taga, G., 1995. A model of the neuro-musculo-skeletal system for human locomotion. I. Emergence of basic gait. Biol. Cybern. 73 (2), 97-111]. In support, he presented a neuromuscular model of human locomotion that combines a CPG with sensory feedback and demonstrates how basic gait can emerge from the global entrainment between the rhythmic activities of the neural and of the musculo-skeletal system.
What the actual ratio of central and reflex inputs is that generates the motor output continues to be debated [Pearson, K. G., 2004. Generating the walking gait: role of sensory feedback. Prog Brain Res 143, 123-129; Frigon, A., Rossignol, S., 2006. Experiments and models of sensorimotor interactions during locomotion. Biol Cybern 95 (6), 607-627; Hultborn, H., 2006. Spinal reflexes, mechanisms and concepts: from Eccles to Lundberg and beyond. Prog Neurobiol 78 (3-5), 215-232; Prochazka, A., Yakovenko, S., 2007. The neuromechanical tuning hypothesis. Prog Brain Res 165, 255-265]. For instance, for walking cats, it has been estimated that only about 30 percent of the muscle activity observed in the weight bearing leg extensors can be attributed to muscle reflexes [Prochazka, A., Gritsenko, V, Yakovenko, S., 2002. Sensory control of locomotion: reflexes versus higher-level control. Adv Exp Med Biol 508, 357-367; Donelan, J. M., McVea, D. A., Pearson, K. G., 2009. Force regulation of ankle extensor muscle activity in freely walking cats. J Neurophysiol 101 (1), 360-371].
In humans, the contribution of reflexes to the muscle activities in locomotion seems to be more prominent. Sinkjaer and colleagues estimated from unloading experiments that reflexes contribute about 50 percent to the soleus muscle activity during stance in walking [Sinkjaer, T., Andersen, J. B., Ladouceur, M., Christensen, L. O., Nielsen, J. B., 2000. Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man. J Physiol 523 Pt 3, 817-827]. More recently, Grey and colleagues found that the soleus activity changes proportionally to changes in the Achilles tendon force, suggesting a direct relationship between positive force feedback and activity for this muscle [Grey, M. J., Nielsen, J. B., Mazzaro, N., Sinkjaer, T., 2007. Positive force feedback in human walking. J Physiol 581 (1), 99-105]. Whether such a large reflex contribution is present for all leg muscles remains open. Perhaps a proximo-distal gradient exists in motor control where proximal leg muscles are mainly controlled by central inputs while distal leg muscles are dominated by reflex inputs due to higher proprioceptive feedback gains and a larger sensitivity to mechanical effects, as Daley and colleagues concluded from locomotion experiments with birds [Daley, M. A., Felix, G., Biewener, A. A., 2007. Running stability is enhanced by a proximo-distal gradient in joint neuromechanical control. J Exp Biol 210 (Pt 3), 383-394].
Adaptation to terrain is an important aspect of walking. Today's commercially-available ankle-foot prostheses utilize lightweight, passive structures that are designed to present appropriate elasticity during the stance phase of walking [S. Ron, Prosthetics and Orthotics: Lower Limb and Spinal. Lippincott Williams & Wilkins 2002]. The advanced composites used in these devices permit some energy storage during controlled dorsiflexion and plantar flexion, and subsequent energy release during powered plantar flexion, much like the Achilles tendon in the intact human [A. L. Hof, B. A. Geelen, Jw. Van den Berg, “Calf muscle moment, work and efficiency in level walking; role of series elasticity,” Journal of Biomechanics, Vol. 16, No. 7, pp. 523-537, 1983; D. A. Winter, “Biomechanical motor pattern in normal walking,” Journal of Motor Behavior, Vol. 15, No. 4, pp. 302-330, 1983].
Although this passive-elastic behavior is a good approximation to the ankle's function during slow walking, normal and fast walking speeds require the addition of external energy, and thus cannot be implemented by any passive ankle-foot device [M. Palmer, “Sagittal plane characterization of normal human ankle function across a range of walking gait speeds,” Master's Thesis, Massachusetts Institute of Technology, Cambridge, Mass., 2002; D. H. Gates, “Characterizing ankle function during stair ascent, descent, and level walking for ankle prosthesis and orthosis design,” Master's Thesis, Boston University, 2004; A. H. Hansen, D. S. Childress, S. C. Miff, S. A. Gard, K. P. Mesplay, “The human ankle during walking: implication for the design of biomimetic ankle prosthesis,” Journal of Biomechanics, Vol. 37, Issue 10, pp. 1467-1474, 2004]. This deficiency is reflected in the gait of transtibial amputees using passive ankle-foot prostheses. Their self-selected walking speed is slower, and stride length shorter, than normal [D. A. Winter and S. E. Sienko. “Biomechanics of below-knee amputee gait,” Journal of Biomechanics, 21, pp. 361-367, 1988]. In addition, their gait is distinctly asymmetric: the range of ankle movement on the unaffected side is smaller [H. B. Skinner and D. J. Effeney, “Gait analysis in amputees,” Am J Phys Med, Vol. 64, pp. 82-89, 1985; H. Bateni and S. Olney, “Kinematic and kinetic variations of below-knee amputee gait,” Journal of Prosthetics & Orthotics, Vol. 14, No. 1, pp. 2-13, 2002], while, on the affected side, the hip extension moment is greater and the knee flexion moment is smaller [D. A. Winter and S. E. Sienko. “Biomechanics of below-knee amputee gait,” Journal of Biomechanics, 21, pp. 361-367, 1988; H. Bateni and S. Olney, “Kinematic and kinetic variations of below-knee amputee gait,” Journal of Prosthetics & Orthotics, Vol. 14, No. 1, pp. 2-13, 2002]. They also expend greater metabolic energy walking than non-amputees [N. H. Molen, “Energy/speed relation of below-knee amputees walking on motor-driven treadmill,” Int. Z. Angew, Physio, Vol. 31, p 173, 1973; G. R. Colborne, S. Naumann, P. E. Longmuir, and D. Berbrayer, “Analysis of mechanical and metabolic factors in the gait of congenital below knee amputees,” Am. J. Phys. Med. Rehabil., Vol. 92, pp 272-278, 1992; R. L. Waters, J. Perry, D. Antonelli, H. Hislop. “Energy cost of walking amputees: the influence of level of amputation,” J Bone Joint Surg. Am., Vol. 58, No. 1, pp. 4246, 1976; E. G. Gonzalez, P. J. Corcoran, and L. R. Rodolfo. Energy expenditure in B/K amputees: correlation with stump length. Archs. Phys. Med. Rehabil. 55, 111-119, 1974; D. J. Sanderson and P. E. Martin. “Lower extremity kinematic and kinetic adaptations in unilateral below-knee amputees during walking,” Gait and Posture. 6, 126-136, 1997; A. Esquenazi, and R. DiGiacomo. “Rehabilitation After Amputation,” Journ Am Podiatr Med Assoc, 91(1): 13-22, 2001]. These differences could possibly be a result of the amputees' greater use of hip power to compensate for the lack of ankle power [A. D. Kuo, “Energetics of actively powered locomotion using the simplest walking model,” J Biomech Eng., Vol. 124, pp. 113-120, 2002; A. D. Kuo, J. M. Donelan, and A. Ruina, “Energetic consequences of walking like an inverted pendulum: Step-sto-step transitions,” Exerc. Sport Sci. Rev., Vol. 33, No. 2, pp. 88-97, 2005; A. Ruina, J. E. Bertram, and M. Srinivasan, “A collisional model of the energetic cost of support work qualitatively explains leg sequencing in walking and galloping, pseudo-elastic leg behavior in running and the walk-to-run transition.” J. Theor. Biol., Vol. 237, No. 2, pp. 170-192, 2005].
Passive ankle-foot prostheses cannot provide the capability of adaptation to terrain. To provide for a normal, economical gait beyond slow walking speeds, powered ankle-foot prostheses have now been developed [S. Au and H. Herr. “Initial experimental study on dynamic interaction between an amputee and a powered ankle-foot prosthesis,” Workshop on Dynamic Walking: Mechanics and Control of Human and Robot Locomotion, Ann Arbor, Mich., May 2006; S. K. Au, J. Weber, and H. Herr, “Biomechanical design of a powered ankle-foot prosthesis,” Proc. IEEE Int. Conf. On Rehabilitation Robotics, Noordwijk, The Netherlands, pp. 298-303, June 2007; S. Au, J. Weber, E. Martinez-Villapando, and H. Herr. “Powered Ankle-Foot Prosthesis for the Improvement of Amputee Ambulation,” IEEE Engineering in Medicine and Biology International Conference. August 23-26, Lyon, France, pp. 3020-3026, 2007; H. Herr, J. Weber, S. Au. “Powered Ankle-Foot Prosthesis,” Biomechanics of the Lower Limb in Health, Disease and Rehabilitation. September 3-5, Manchester, England, pp. 72-74, 2007; S. K. Au, “Powered Ankle-Foot Prosthesis for the Improvement of Amputee Walking Economy,” Ph.D. Thesis, Massachusetts Institute of Technology, Cambridge, Mass., 2007; S. Au, J. Weber, and H. Herr. “Powered Ankle-foot Prosthesis Improves Walking Metabolic Economy,” IEEE Trans. on Robotics, Vol. 25, pp. 51-66, 2009; J. Hitt, R. Bellman, M. Holgate, T. Sugar, and K. Hollander, “The sparky (spring ankle with regenerative kinetics) projects: Design and analysis of a robotic transtibial prosthesis with regenerative kinetics,” in Proc. IEEE Int. Conf. Robot. Autom., Orlando, Fla., pp 2939-2945, May 2006; S. K. Au, H. Herr, “On the Design of a Powered Ankle-Foot Prosthesis: The Importance of Series and Parallel Elasticity,” IEEE Robotics & Automation Magazine. pp. 52-59, September 2008]. Some of these are of size and weight comparable to the intact human ankle-foot, and have the elastic energy storage, motor power, and battery energy to provide for a day's typical walking activity [S. K. Au, H. Herr, “On the Design of a Powered Ankle-Foot Prosthesis: The Importance of Series and Parallel Elasticity,” IEEE Robotics & Automation Magazine. pp. 52-59, September 2008].
The use of active motor power in these prostheses raises the issue of control. In previous work with these powered devices, the approach taken was to match the torque-ankle state profile of the intact human ankle for the activity to be performed [S. K. Au, “Powered Ankle-Foot Prosthesis for the Improvement of Amputee Walking Economy,” Ph.D. Thesis, Massachusetts Institute of Technology, Cambridge, Mass., 2007; J. Hitt, R. Bellman, M. Holgate, T. Sugar, and K. Hollander, “The sparky (spring ankle with regenerative kinetics) projects: Design and analysis of a robotic transtibial prosthesis with regenerative kinetics,” in Proc. IEEE Int. Conf. Robot. Autom., Orlando, Fla., pp 2939-2945, May 2006; F. Sup, A. Bohara, and M. Goldfarb, “Design and Control of a Powered Transfemoral Prosthesis,” The International Journal of Robotics Research, Vol. 27, No. 2, pp. 263-273, 2008]. The provision of motor power meant that the open work loops of the angle-torque profiles in faster walking could be supported, rather than just the spring-like behavior provided by passive devices. However, this control approach exhibited no inherent adaptation. Instead, torque profiles were required for all intended activities and variation of terrain, along with an appropriate means to select among them.
In general, existing commercially available active ankle prostheses are only able to reconfigure the ankle joint angle during the swing phase, requiring several strides to converge to a terrain-appropriate ankle position at first ground contact. Further, they do not provide any of the stance phase power necessary for normal gait, and therefore cannot adapt net stance work with terrain slope. In particular, control schemes for powered ankle-foot prostheses rely upon fixed torque-ankle state relationships obtained from measurements of intact humans walking at target speeds and across known terrains. Although effective at their intended gait speed and terrain, these controllers do not allow for adaptation to environmental disturbances such as speed transients and terrain variation.
Neuromuscular models with a positive force feedback reflex scheme as the basis of control have recently been employed in simulation studies of the biomechanics of legged locomotion [H. Geyer, H. Herr, “A muscle-reflex model that encodes principles of legged mechanics predicts human walking dynamics and muscle activities,” (Submitted for publication); H. Geyer, A. Seyfarth, R. Blickhan, “Positive force feedback in bouncing gaits?,” Proc. R Society. Lond. B 270, pp. 2173-2183, 2003]. Such studies show promise regarding the need for terrain adaptation.